Protective Strategies of Haberlea rhodopensis for Acquisition of Freezing Tolerance: Interaction between Dehydration and Low Temperature
Abstract
:1. Introduction
2. Results
2.1. Freezing Temperature and Molecular Mobility in Winter Leaves of Haberlea Rhodopensis
2.2. Changes in Electrolyte Leakage and MDA Content during Cold Acclimation, Freezing Stress and Freezing-Induced Desiccation
2.2.1. Electrolyte Leakage (EL)
2.2.2. Malondialdehyde (MDA)
2.3. Changes in Fatty Acids Profile under CA, Freezing Stress, and Freezing-Induced Desiccation
2.4. Importance of Proline and Carbohydrates for Freezing Tolerance
2.4.1. Proline
2.4.2. Carbohydrates
2.5. The Role of Protective Proteins for Freezing Tolerance of H. Rhodopensis
2.5.1. Dehydrins
2.5.2. ELIPs
2.6. Correlation Patterns among Physiological and Biochemical Parameters
3. Discussion
3.1. Changes in Membrane Lipids Composition Contribute to Freezing Tolerance
3.2. The Role of Proline and Soluble Sugars in Freezing Tolerance
3.3. The Protective Role of Dehydrins and ELIPs during Freezing Stress
4. Materials and Methods
4.1. Plant Material and Temperature Treatments
- (1)
- Cold acclimation (CA): plants were sampled during gradual acclimation to low daily mean temperatures ranging from +1 °C to +7 °C (dates 7–28 November; CA).
- (2)
- Freezing stress (FS): after an overnight freezing wave exposure to ca. −10 °C, resulting in a slight desiccation of the leaves (ca. 25% reduction in RWC compared to the control) on the sampling day (date 30 November).
- (3)
- Freezing stress + desiccation (FS + D): plants were sampled during long-term exposure to freezing temperatures when significant desiccation of the leaves occurred (RWC ranging from 10 to 20%) from the beginning of December 2016 (date 1 December) till the end of January (date 30 January); During December, nighttime temperatures were negative, and the average daily temperature was ca. +5 °C, while in January for more than 20 days minimum temperatures reached values in the range of −8 °C to −17 °C. As a consequence, sampling on date 30 January is representative of long-term exposure to freezing temperatures compared to December samplings.
- (4)
- Recovery (R): plants were sampled in March 2017 as representative of plant recovery from freezing-induced desiccation.
4.2. Relative Water Content (RWC)
4.3. Dynamic Mechanical Thermal Analysis (DMTA)
4.4. Differential Scanning Calorimetry (DSC)
4.5. Electrolyte Leakage
4.6. Malondialdehyde Content (MDA)
4.7. Proline Content
4.8. Carbohydrate Analysis
4.9. Fatty Acid Analysis
4.10. Total Leaf Protein Extraction, SDS-PAGE and Western Blot Analysis
4.11. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Control | CA | FS | FS + D | R | ||||
---|---|---|---|---|---|---|---|---|
Fatty acid | 5 May | 7 November | 28 November | 30 November | 5 December | 8 December | 14 December | 22 March |
RWC 86% | RWC 80% | RWC 82% | RWC 65% | RWC 35% | RWC 20% | RWC 12% | RWC 86% | |
Palmitic (16:0) | 40.36 ± 1.54 d | 38.84 ± 0.65 cd | 36.45 ± 1.02 bc | 36.77 ± 2.73 bc | 36.73 ± 0.11 bc | 36.38 ± 0.90 bc | 27.61 ± 2.74 a | 35.47 ± 0.60 b |
Palmitoleic (16:1) | 0.34 ± 0.01 d | 0.12 ± 0.02 ab | 0.15 ± 0.01 b | 0.34 ± 0.08 d | 0.06 ± 0.01 a | 0.16 ± 0.01 b | 0.24 ± 0.04 c | 0.59 ± 0.04 e |
Stearic (18:0) | 28.81 ± 1.63 b | 29.88 ± 1.14 b | 32.30 ± 1.70 b | 23.82 ± 1.02 a | 24.42 ± 1.25 a | 24.53 ± 0.49 a | 22.93 ± 3.23 a | 24.67 ± 2.84 a |
Oleic (18:1) | 12.87 ± 1.56 d | 9.61 ± 0.31 bc | 9.61 ± 0.63 bc | 16.57 ± 1.84 e | 5.97 ± 0.80 a | 6.06 ± 0.15 a | 7.58 ± 1.32 ab | 10.32 ± 1.52 c |
Linoleic (18:2) | 12.51 ± 1.43 a | 14.22 ± 0.88 ab | 12.50 ± 1.14 a | 12.60 ± 1.91 a | 16.61 ± 2.13 bc | 18.23 ± 0.30 c | 23.20 ± 4.23 d | 17.21 ± 1.33 bc |
Linolenic (18:3) | 4.20 ± 0.48 a | 6.74 ± 0.75 ab | 8.01 ± 1.61 b | 9.17 ± 1.62 bc | 15.68 ± 2.24 de | 14.28 ± 0.78 d | 17.57 ± 2.43 e | 11.09 ± 1.96 c |
Arachidic (20:0) | 0.53 ± 0.07 cd | 0.51 ± 0.03 c | 0.45 ± 0.02 bc | 0.66 ± 0.07 e | 0.44 ± 0.01 bc | 0.13 ± 0.02 a | 0.64 ± 0.10 de | 0.36 ± 0.05 b |
Behenic (22:0) | 0.28 ± 0.05 b | 0.09 ± 0.01 a | 0.53 ± 0.08 c | 0.07 ± 0.02 a | 0.08 ± 0.01 a | 0.23 ± 0.01 b | 0.23 ± 0.05 b | 0.31 ± 0.10 b |
Control | CA | FS* | FS + D | R | |||||
---|---|---|---|---|---|---|---|---|---|
Group | Compounds | 5 May | 7 November | 28 November | 30 November | 5 December | 8 December | 14 December | 22 March |
RWC 86% | RWC 80% | RWC 82% | RWC 65% | RWC 35% | RWC 20% | RWC 12% | RWC 86% | ||
Carbohydrates | Raffinose | 1.00 | 1.16 | 1.44 | 2.81 | 1.84 | 6.84 | 16.53 | 0.71 |
Sucrose | 1.00 | 0.85 | 1.54 | 1.17 | 2.93 | 4.36 | 15.87 | 1.13 | |
Glucose | 1.00 | 2.58 | 3.91 | 4.22 | 6.09 | 8.56 | 5.07 | 2.79 | |
Fructose | 1.00 | 1.76 | 3.41 | 3.06 | 4.42 | 8.00 | 5.16 | 2.23 | |
Galactose | 1.00 | 2.12 | 2.31 | 4.07 | 3.31 | 3.31 | 2.14 | 2.74 | |
Inositol | 1.00 | 2.44 | 2.87 | 1.72 | 2.58 | 2.89 | 2.83 | 2.81 | |
Organic acids | Malic acid | 1.00 | 1.41 | 1.48 | 0.61 | 2.43 | 3.12 | 3.51 | 1.03 |
Citric acid | 1.00 | 1.38 | 1.37 | 0.42 | 1.29 | 1.28 | 3.15 | 1.10 |
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Georgieva, K.; Mihailova, G.; Fernández-Marín, B.; Bertazza, G.; Govoni, A.; Arzac, M.I.; Laza, J.M.; Vilas, J.L.; García-Plazaola, J.I.; Rapparini, F. Protective Strategies of Haberlea rhodopensis for Acquisition of Freezing Tolerance: Interaction between Dehydration and Low Temperature. Int. J. Mol. Sci. 2022, 23, 15050. https://doi.org/10.3390/ijms232315050
Georgieva K, Mihailova G, Fernández-Marín B, Bertazza G, Govoni A, Arzac MI, Laza JM, Vilas JL, García-Plazaola JI, Rapparini F. Protective Strategies of Haberlea rhodopensis for Acquisition of Freezing Tolerance: Interaction between Dehydration and Low Temperature. International Journal of Molecular Sciences. 2022; 23(23):15050. https://doi.org/10.3390/ijms232315050
Chicago/Turabian StyleGeorgieva, Katya, Gergana Mihailova, Beatriz Fernández-Marín, Gianpaolo Bertazza, Annalisa Govoni, Miren Irati Arzac, José Manuel Laza, José Luis Vilas, José Ignacio García-Plazaola, and Francesca Rapparini. 2022. "Protective Strategies of Haberlea rhodopensis for Acquisition of Freezing Tolerance: Interaction between Dehydration and Low Temperature" International Journal of Molecular Sciences 23, no. 23: 15050. https://doi.org/10.3390/ijms232315050